Biomarkers of oxidative stress, biochemical changes, and the activity of lysosomal enzymes in the livers of rainbow trout (Oncorhynchus mykiss Walbaum) vaccinated against yersiniosis before a Yersinia ruckeri challenge
Department of Preclinical Sciences and Infectious Diseases, Faculty of Veterinary Medicine and Animal Sciences, Poznań University of Life SciencesPoznań, Poland
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.
Barnes A.C.: Chapter 13, Enteric Redmouth Disease (ERM) (Yersinia ruckeri). In: Fish diseases and disorders, Volume 3, Viral, bacterial and fungal infections, Third Edition, edited by P.T.K. Woo, J.F. Leatherland, D.W. Bruno, CAB International Publishing, Wallingford, UK, 2011, pp. 484–511.BarnesA.C.: Chapter 13, Enteric Redmouth Disease (ERM) (Yersinia ruckeri). In: Fish diseases and disorders, Volume 3, Viral, bacterial and fungal infections, Third Edition, edited by WooP.T.K.LeatherlandJ.F.BrunoD.W., CAB International Publishing, Wallingford, UK, 2011, pp. 484–511.Search in Google Scholar
Barrett A.J., Heath M.F.: Lysosomal enzymes. In: Lysosomes, a Laboratory Handbook, edited by J.T. Dingle, North-Holland Publishing Company, New York, NY, USA, 1977, pp. 19–146.BarrettA.J.HeathM.F.: Lysosomal enzymes. In: Lysosomes, a Laboratory Handbook, edited by DingleJ.T.North-Holland Publishing Company, New York, NY, USA, 1977, pp. 19–146.Search in Google Scholar
Bassoy E.Y., Walch M., Martinvalet D.: Reactive Oxygen Species: Do They Play a Role in Adaptive Immunity? Front Immunol 2021, 12, 755856, doi: 10.3389/fimmu.2021.755856.BassoyE.Y.WalchM.MartinvaletD.: Reactive Oxygen Species: Do They Play a Role in Adaptive Immunity?Front Immunol2021, 12, 755856, doi: 10.3389/fimmu.2021.755856.Open DOISearch in Google Scholar
Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72, 248–254, doi: 10.1006/abio.1976.9999.BradfordM.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem1976, 72, 248–254, doi: 10.1006/abio.1976.9999.Open DOISearch in Google Scholar
Bridle A.R., Koop B.F., Nowak B.F.: Identification of surrogates of protection against yersiniosis in immersion vaccinated Atlantic salmon. PLoS One 2012, 7, e40841, doi: 10.1371/journal.pone.0040841.BridleA.R.KoopB.F.NowakB.F.: Identification of surrogates of protection against yersiniosis in immersion vaccinated Atlantic salmon. PLoS One2012, 7, e40841, doi: 10.1371/journal.pone.0040841.Open DOISearch in Google Scholar
Cadenas E., Davies K.J.: Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000, 29, 222–230, doi: 10.1016/s0891-5849(00)00317-8.CadenasE.DaviesK.J.: Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med2000, 29, 222–230, doi: 10.1016/s0891-5849(00)00317-8.Open DOISearch in Google Scholar
Chelikani P., Fita I., Loewen P.C.: Diversity of structures and properties among catalases. Cell Mol Life Sci 2004, 61, 92–208, doi: 10.1007/s00018-003-3206-5.ChelikaniP.FitaI.LoewenP.C.: Diversity of structures and properties among catalases. Cell Mol Life Sci2004, 61, 92–208, doi: 10.1007/s00018-003-3206-5.Open DOISearch in Google Scholar
Chettri J.K., Raida M.K., Kania P.W., Buchmann K.: Differential immune response of rainbow trout ( Oncorhynchus mykiss) at early developmental stages (larvae and fry) against the bacterial pathogen Yersinia ruckeri. Dev Comp Immunol 2012, 36, 463–474, doi: 10.1016/j.dci.2011.08.014.ChettriJ.K.RaidaM.K.KaniaP.W.BuchmannK.: Differential immune response of rainbow trout ( Oncorhynchus mykiss) at early developmental stages (larvae and fry) against the bacterial pathogen Yersinia ruckeri. Dev Comp Immunol2012, 36, 463–474, doi: 10.1016/j.dci.2011.08.014.Open DOISearch in Google Scholar
DeMartino G.N., Goldberg A.L.: Thyroid hormones control lysosomal enzyme activities in liver and skeletal muscle. Proc Natl Acad Sci U S A 1978, 75, 1369–1373, doi: 10.1073/pnas.75.3.1369.DeMartinoG.N.GoldbergA.L.: Thyroid hormones control lysosomal enzyme activities in liver and skeletal muscle. Proc Natl Acad Sci U S A1978, 75, 1369–1373, doi: 10.1073/pnas.75.3.1369.Open DOISearch in Google Scholar
Deshmukh S., Raida M.K., Dalsgaard I., Chettri J.K., Kania P.W., Buchmann K.: Comparative protection of two different commercial vaccines against Yersinia ruckeri serotype O1 and biotype 2 in rainbow trout (Oncorhynchus mykiss). Vet Immunol Immunopathol 2012, 145, 379–385, doi: 10.1016/j.vetimm.2011.12.014.DeshmukhS.RaidaM.K.DalsgaardI.ChettriJ.K.KaniaP.W.BuchmannK.: Comparative protection of two different commercial vaccines against Yersinia ruckeri serotype O1 and biotype 2 in rainbow trout (Oncorhynchus mykiss). Vet Immunol Immunopathol2012, 145, 379–385, doi: 10.1016/j.vetimm.2011.12.014.Open DOISearch in Google Scholar
Evenhuis J.P., Cleveland B.M.: Modulation of rainbow trout (Oncorhynchus mykiss) intestinal immune gene expression following bacterial challenge. Vet Immunol Immunopathol 2012, 146, 8–17, doi: 10.1016/j.vetimm.2012.01.008.EvenhuisJ.P.ClevelandB.M.: Modulation of rainbow trout (Oncorhynchus mykiss) intestinal immune gene expression following bacterial challenge. Vet Immunol Immunopathol2012, 146, 8–17, doi: 10.1016/j.vetimm.2012.01.008.Open DOISearch in Google Scholar
Galaktionova L.P., Molchanov A.V., El’chaninova S.A., Varshavskiĭ B.: Sostoianie perekisnogo okisleniia u bol’nykh s iazvennoĭ bolezn’iu zheludka i dvenadtsatiperstnoĭ kishki (Lipid peroxidation in patients with gastric and duodenal peptic ulcers – in Russian). Klin Lab Diagn 1998, 6, 10–14.GalaktionovaL.P.MolchanovA.V.El’chaninovaS.A.VarshavskiĭB.: Sostoianie perekisnogo okisleniia u bol’nykh s iazvennoĭ bolezn’iu zheludka i dvenadtsatiperstnoĭ kishki (Lipid peroxidation in patients with gastric and duodenal peptic ulcers – in Russian). Klin Lab Diagn1998, 6, 10–14.Search in Google Scholar
Ghosh B., Nguyen T.D., Crosbie P.B.B., Nowak B.F., Bridle A.R.: Oral vaccination of first-feeding Atlantic salmon, Salmo salar L., confers greater protection against yersiniosis than immersion vaccination. Vaccine 2016, 34, 599–608, doi: 10.1016/j.vaccine.2015.12.044.GhoshB.NguyenT.D.CrosbieP.B.B.NowakB.F.BridleA.R.: Oral vaccination of first-feeding Atlantic salmon, Salmo salar L., confers greater protection against yersiniosis than immersion vaccination. Vaccine2016, 34, 599–608, doi: 10.1016/j.vaccine.2015.12.044.Open DOISearch in Google Scholar
Glatzle D., Vuilleumier J. P., Weber F., Decker K.: Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in humans. Experientia 1974, 30, 665–667, doi: 10.1007/BF01921531.GlatzleD.VuilleumierJ. P., WeberF.DeckerK.: Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in humans. Experientia1974, 30, 665–667, doi: 10.1007/BF01921531.Open DOISearch in Google Scholar
Herasimov I., Plaksina O.: Non-enzymatic determination of lactate and pyruvate concentrations in blood sample (in Ukrainian). Laboratorna Diagnostyka 2000, 1, 46–48.HerasimovI.PlaksinaO.: Non-enzymatic determination of lactate and pyruvate concentrations in blood sample (in Ukrainian). Laboratorna Diagnostyka2000, 1, 46–48.Search in Google Scholar
Horne M.T., Barnes A.C.: Chapter 13, Enteric Redmouth Disease (Yersinia ruckeri) In: Fish diseases and disorders, Volume 3, Viral, bacterial and fungal infections, First Edition, edited by P.T.K. Woo, D.W. Bruno, CAB International Publishing, Wallingford, UK, 1999, pp. 445–477.HorneM.T.BarnesA.C.: Chapter 13, Enteric Redmouth Disease (Yersinia ruckeri) In: Fish diseases and disorders, Volume 3, Viral, bacterial and fungal infections, First Edition, edited by WooP.T.K.BrunoD.W., CAB International Publishing, Wallingford, UK, 1999, pp. 445–477.Search in Google Scholar
Ingerslev H.C., Strube M.L., von Gersdorff Jørgensen L., Dalsgaard I., Boye M., Madsen L.: Diet type dictates the gut microbiota and the immune response against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 2014, 40, 624–633, doi: 10.1016/j.fsi.2014.08.021.IngerslevH.C.StrubeM.L.von Gersdorff JørgensenL.DalsgaardI.BoyeM.MadsenL.: Diet type dictates the gut microbiota and the immune response against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol2014, 40, 624–633, doi: 10.1016/j.fsi.2014.08.021.Open DOISearch in Google Scholar
Kamyshnikov V.: Determination of the content of TBA active substances (malondialdehyde) in blood erythrocytes. In: Reference Book for Clinical and Biochemical Research and Laboratory Diagnostics (in Russian). MED Press-inform, Moscow, 2009, pp. 549-550.KamyshnikovV.: Determination of the content of TBA active substances (malondialdehyde) in blood erythrocytes. In: Reference Book for Clinical and Biochemical Research and Laboratory Diagnostics (in Russian). MED Press-inform, Moscow, 2009, pp. 549–550.Search in Google Scholar
Koroliuk M.A., Ivanova L.I., Maĭorova I.G., Tokarev V.E.: Metod opredeleniia aktivnosti katalazy (A method of determining catalase activity – in Russian). Lab Delo 1988, 1, 16–19.KoroliukM.A.IvanovaL.I.MaĭorovaI.G.TokarevV.E.: Metod opredeleniia aktivnosti katalazy (A method of determining catalase activity – in Russian). Lab Delo1988, 1, 16–19.Search in Google Scholar
Kostiuk V.A., Potapovich A.I., Kovaleva Zh.V.: Prostoĭ i chuvstvitel’nyĭ metod opredeleniia aktivnosti superoksid-dismutazy, osnovannyĭ na reaktsii okisleniia kvertsetina (A simple and sensitive method of determination of superoxide dismutase activity based on the reaction of quercetin oxidation – in Russian). Vopr Med Khim 1990, 36, 88–91.KostiukV.A.PotapovichA.I.KovalevaZh.V.: Prostoĭ i chuvstvitel’nyĭ metod opredeleniia aktivnosti superoksid-dismutazy, osnovannyĭ na reaktsii okisleniia kvertsetina (A simple and sensitive method of determination of superoxide dismutase activity based on the reaction of quercetin oxidation – in Russian). Vopr Med Khim1990, 36, 88–91.Search in Google Scholar
Kumar G., Hummel K., Noebauer K., Welch T.J., Razzazi-Fazeli E., El-Matbouli M.: Proteome analysis reveals a role of rainbow trout lymphoid organs during Yersinia ruckeri infection process. Sci Rep 2018, 8, 13998, doi: 10.1038/s41598-018-31982-6.KumarG.HummelK.NoebauerK.WelchT.J.Razzazi-FazeliE.El-MatbouliM.: Proteome analysis reveals a role of rainbow trout lymphoid organs during Yersinia ruckeri infection process. Sci Rep2018, 8, 13998, doi: 10.1038/s41598-018-31982-6.Open DOISearch in Google Scholar
Kumar G., Menanteau-Ledouble S., Saleh M., El-Matbouli M.: Yersinia ruckeri, the causative agent of enteric redmouth disease in fish. Vet Res 2015, 46, 103, doi: 10.1186/s13567-015-0238-4.KumarG.Menanteau-LedoubleS.SalehM.El-MatbouliM.: Yersinia ruckeri, the causative agent of enteric redmouth disease in fish. Vet Res2015, 46, 103, doi: 10.1186/s13567-015-0238-4.Open DOISearch in Google Scholar
Kurhaluk N., Tkachenko H.: Antioxidants, lysosomes and elements status during the life cycle of sea trout Salmo trutta m. trutta L. Sci Rep 2021, 11, 5545, doi: 10.1038/s41598-021-85127-3.KurhalukN.TkachenkoH.: Antioxidants, lysosomes and elements status during the life cycle of sea trout Salmo trutta m. trutta L. Sci Rep2021, 11, 5545, doi: 10.1038/s41598-021-85127-3.Open DOISearch in Google Scholar
Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., Ahn B.W., Shaltiel S., Stadtman E.R.: Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990, 186, 464–478, doi: 10.1016/0076-6879(90)86141-h.LevineR.L.GarlandD.OliverC.N.AmiciA.ClimentI.LenzA.G.AhnB.W.ShaltielS.StadtmanE.R.: Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol1990, 186, 464–478, doi: 10.1016/0076-6879(90)86141-h.Open DOISearch in Google Scholar
Liu T., Wang E., Wei W., Wang K., Yang Q., Ai X.: TcpA, a novel Yersinia ruckeri TIR-containing virulent protein mediates immune evasion by targeting MyD88 adaptors. Fish Shellfish Immunol 2019, 94, 58–65, doi: 10.1016/j.fsi.2019.08.069.LiuT.WangE.WeiW.WangK.YangQ.AiX.: TcpA, a novel Yersinia ruckeri TIR-containing virulent protein mediates immune evasion by targeting MyD88 adaptors. Fish Shellfish Immunol2019, 94, 58–65, doi: 10.1016/j.fsi.2019.08.069.Open DOISearch in Google Scholar
McDonald J.K., Barrett A.J.: Exopeptidases. In: Mammalian Proteinases: A Glossary and Bibliography, edited by A.J. Barrett, J.K. McDonald, Academic Press, London, UK, 1986, pp. 114–144.McDonaldJ.K.BarrettA.J.: Exopeptidases. In: Mammalian Proteinases: A Glossary and Bibliography, edited by BarrettA.J.McDonaldJ.K., Academic Press, London, UK, 1986, pp. 114–144.Search in Google Scholar
Mittal M., Siddiqui M.R., Tran K., Reddy S.P., Malik A.B.: Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 2014, 20,1126–1167, doi: 10.1089/ars.2012.5149.MittalM.SiddiquiM.R.TranK.ReddyS.P.MalikA.B.: Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal2014, 20, 1126–1167, doi: 10.1089/ars.2012.5149.Open DOISearch in Google Scholar
Moin V.M.: Prostoĭ i spetsificheskiĭ metod opredeleniia aktivnosti glutationperoksidazy v éritrotsitakh (A simple and specific method for determining glutathione peroxidase activity in erythrocytes – in Russian). Lab Delo 1986 12, 724–727.MoinV.M.: Prostoĭ i spetsificheskiĭ metod opredeleniia aktivnosti glutationperoksidazy v éritrotsitakh (A simple and specific method for determining glutathione peroxidase activity in erythrocytes – in Russian). Lab Delo1986, 12, 724–727.Search in Google Scholar
Reitman S., Frankel S.: A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 1957, 28, 56–63, doi: 10.1093/ajcp/28.1.56.ReitmanS.FrankelS.: A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol1957, 28, 56–63, doi: 10.1093/ajcp/28.1.56.Open DOISearch in Google Scholar
Sevela M., Tovarek J.: Metoda stanovení laktikodehydrogenázy v télních tekutinách (Method for the estimation of lactic dehydrogenase – in Czech). Cas Lek Cesk 1959, 98, 27, 844–848.SevelaM.TovarekJ.: Metoda stanovení laktikodehydrogenázy v télních tekutinách (Method for the estimation of lactic dehydrogenase – in Czech). Cas Lek Cesk1959, 98, 27, 844–848.Search in Google Scholar
Spooner R., Yilmaz O.: The role of reactive-oxygen-species in microbial persistence and inflammation. Int J Mol Sci 2011, 12, 334–352, doi: 10.3390/ijms12010334.SpoonerR.YilmazO.: The role of reactive-oxygen-species in microbial persistence and inflammation. Int J Mol Sci2011, 12, 334–352, doi: 10.3390/ijms12010334.Open DOISearch in Google Scholar
Stanisz A.: An accessible statistics course using STATISTICA PL with examples from medicine; Volume 1, Basic statistics; Volume 2, Linear and non-linear models; Volume 3, Multivariate analyses, StatSoft Polska, Krakow, 2006, 2007, pp. 532, pp. 868, pp. 500.StaniszA.: An accessible statistics course using STATISTICA PL with examples from medicine; Volume 1, Basic statistics; Volume 2, Linear and non-linear models; Volume 3, Multivariate analyses, StatSoft Polska, Krakow,2006, 2007, pp. 532, pp. 868, pp. 500.Search in Google Scholar
Tobback E., Decostere A., Hermans K., Haesebrouck F., Chiers K.: Yersinia ruckeri infections in salmonid fish. J Fish Dis 2007, 30, 257–268, doi: 10.1111/j.1365-2761.2007.00816.x.TobbackE.DecostereA.HermansK.HaesebrouckF.ChiersK.: Yersinia ruckeri infections in salmonid fish. J Fish Dis2007, 30, 257–268, doi: 10.1111/j.1365-2761.2007.00816.x.Open DOISearch in Google Scholar
Villumsen K.R., Neumann L., Ohtani M., Strøm H.K., Raida M.K.: Oral and anal vaccination confers full protection against enteric redmouth disease (ERM) in rainbow trout. PLoS One 2014, 9, e93845, doi: 10.1371/journal.pone.0093845.VillumsenK.R.NeumannL.OhtaniM.StrømH.K.RaidaM.K.: Oral and anal vaccination confers full protection against enteric redmouth disease (ERM) in rainbow trout. PLoS One2014, 9, e93845, doi: 10.1371/journal.pone.0093845.Open DOISearch in Google Scholar
Wheeler R.W., Davies R.L., Dalsgaard I., Garcia J., Welch T.J., Wagley S., Bateman K.S., Verner-Jeffreys D.W.: Yersinia ruckeri biotype 2 isolates from mainland Europe and the UK likely represent different clonal groups. Dis Aquat Organ 2009, 84, 25–33, doi: 10.3354/dao02039.WheelerR.W.DaviesR.L.DalsgaardI.GarciaJ.WelchT.J.WagleyS.BatemanK.S.Verner-JeffreysD.W.: Yersinia ruckeri biotype 2 isolates from mainland Europe and the UK likely represent different clonal groups. Dis Aquat Organ2009, 84, 25–33, doi: 10.3354/dao02039.Open DOISearch in Google Scholar
Younus H.: Therapeutic potentials of superoxide dismutase. Int J Health Sci (Qassim) 2018, 12, 88–93.YounusH.: Therapeutic potentials of superoxide dismutase. Int J Health Sci (Qassim)2018, 12, 88–93.Search in Google Scholar